Development of foregut and proboscis in the buccinid neogastropod Nassarius mendicus: Evolutionary opportunity exploited by a developmental module

Abstract

This article extends previous descriptions of foregut development and metamorphosis in neogastropods by providing data on the buccinid Nassarius mendicus, a species with a feeding larva. Histological sections showed that, like many other gastropods, the postmetamorphic buccal cavity and radular sac of N. mendicus differentiate during the larval stage from a ventral outpocketing of the distal larval esophagus. However, in N. mendicus the outpocketing also gives rise to the entire anterior esophagus and valve of Leiblein, suggesting that both these structures may be evolutionary derivatives of the gastropod buccal cavity. Scanning electron microscopy and three-dimensional reconstructions of section profiles revealed that the distal larval esophagus and larval mouth are completely destroyed at metamorphosis. The postmetamorphic mouth is formed as a new orifice. Furthermore, epithelia covering the proboscis and proboscis sac arise from preexisting epidermal epithelium of the larval head, an interpretation that contradicts an earlier suggestion on the origin of these epithelial elements in neogastropods with a feeding larval stage. These results, when compared to foregut development in other gastropods, lead me to propose that the gastropod buccal cavity and buccal mass is a developmental module. Canalized development of this module may have been important to the "evolvability" of the complex gastropod foregut, because it allowed a silent developmental novelty to arise (secondary formation of the postmetamorphic mouth) without disrupting development of the whole module. Nevertheless, this silent novelty might have subsequently facilitated dramatic evolutionary change by allowing the elaborate foregut structure of predatory, postmetamorphic neogastropods to arise in late stage larvae without compromising larval feeding.